• 1

    McBride WJ, Bielefelted-Ohmann H, 2000. Dengue viral infections; pathogenesis and epidemiology. Microbes Infect 2 :1041–1050.

  • 2

    Forattini OP, 1986. Identificação de Aedes (Stegomyia) albopictus (Skuse) no Brasil. Rev Saude Publica 20 :244–245.

  • 3

    Ayres CF, Romao TP, Melo-Santos MA, Furtado AF, 2002. Genetic diversity in Brazilian populations of Aedes albopictus.Mem Inst Oswaldo Cruz 97 :871–875.

    • Search Google Scholar
    • Export Citation
  • 4

    Reiter P, Sprenger D, 1987. The used tire trade: a mechanism for the worldwide dispersal of container breeding mosquitoes. J Am Mosq Control Assoc 3 :494–501.

    • Search Google Scholar
    • Export Citation
  • 5

    Craven RB, Eliason DA, Francy DB, Reiter P, Campos EG, Jakob WL, Smith GC, Bozzi CJ, Moore CG, Maupin GO, Monath TP, 1988. Importation of Aedes albopictus and other exotic mosquito species into the United States in used tires from Asia. J Am Mosq Control Assoc 4 :138–142.

    • Search Google Scholar
    • Export Citation
  • 6

    Mitchell CJ, 1995. The role of Aedes albopictus as an arbovirus vector. Parassitologia 37 :109–113.

  • 7

    Ibanez-Bernal S, Briseno B, Mutebi JP, Argot E, Rodriguez G, Martinez-Campos C, Paz R, de la Fuente-San Roman P, Tapia-Conyer R, Flisser A, 1997. First record in America of Aedes albopictus naturally infected with dengue virus during the 1995 outbreak at Reynosa, Mexico. Med Vet Entomol 11 :305–309.

    • Search Google Scholar
    • Export Citation
  • 8

    Miller BR, Ballinger ME, 1988. Aedes albopictus mosquitoes introduced into Brazil: vector competence for yellow fever and dengue viruses. Trans R Soc Trop Med Hyg 82 :476–477.

    • Search Google Scholar
    • Export Citation
  • 9

    Rodhain F, 1995. Aedes albopictus: a potential problem in France. Parassitologia 37 :115–119.

  • 10

    Hawley WA, Pumpuni CB, Brady RH, Graig GB Jr, 1989. Overwintering survival of Aedes albopictus (Diptera: Culicidae) eggs in Indiana. J Med Entomol 26 :122–129.

    • Search Google Scholar
    • Export Citation
  • 11

    Hanson SM, Graig GB Jr, 1994. Cold acclimation, diapause, and geographic origin affect cold hardiness in eggs of Aedes albopictus (Diptera: Culicidae).J Med Entomol 31 :192–201.

    • Search Google Scholar
    • Export Citation
  • 12

    Rawlins SC, Martinez R, Wiltshire S, Legall G, 1998. A comparision of surveillance systems for the dengue vector Aedes aegypti in Port of Spain, Trinidad. J Am Mosq Control Assoc 14 :131–136.

    • Search Google Scholar
    • Export Citation
  • 13

    Pontes RJ, Freeman J, Oliveira-Lima JW, Hodgson JC, Spielman A, 2000. Vector densities that potentiate dengue outbreaks in a Brazilian city. Am J Trop Med Hyg 62 :378–383.

    • Search Google Scholar
    • Export Citation
  • 14

    Ministério da Saúde: Fundação Nacional da Saúde, 2001. Dengue Instruções para Pessoal de Combate ao Vetor: Manual de Normas Técnicas. Revised third edition. Brasília: Ministério da Saúde: Fundação Nacional da Saúde.

  • 15

    Tun-Lin W, Kay BH, Barnes A, 1995. The premise condition index: a tool for streamlining surveys of Aedes aegypti.Am J Trop Med Hyg 53 :591–594.

    • Search Google Scholar
    • Export Citation
  • 16

    Forattini OP, 2002. Culicidologia Médica. Volume 2. São Paulo: Editora da Universidade de São Paulo, 411–415.

  • 17

    Braga IA, Gomes AC, Nelson M, Mello RCG, Bergamaschi DP, Souza JMP, 2000. Comparação entre pesquisa larvária e armadilha de oviposição, para detecção de Aedes aegypti.Ver Soc Bras Med Trop 33 :347–353.

    • Search Google Scholar
    • Export Citation
  • 18

    Marques CCA, Marques GRAM, Brito M, Santos-Neto LG, Ishibashi VC, Gomes FA, 1993. Estudo comparativo de eficácia de larvitrampas e ovitrampas para vigilância de vetores de dengue e febre amarela. Rev Saude Publica 27 :237–241.

    • Search Google Scholar
    • Export Citation
  • 19

    Serufo JC, Oca HM, Tavares VA, Souza AM, Rosa RV, Jamal MC, Lemos JR, Oliveira MA, Nogueira RMR, Schatzmayr HG, 1993. Isolation of dengue virus type 1 from larvae of Aedes albopictus in Campos Altos City, state of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 88 :503–504.

    • Search Google Scholar
    • Export Citation
  • 20

    Shroyer DA, 1990. Vertical maintenance of dengue-1 virus in sequential generation of Aedes albopictus.J Am Mosq Control Assoc 6 :312.

  • 21

    Freier JE, Rosen L, 1987. Vertical transmission of dengue viruses by mosquitoes of the Aedes scutellaris group. Am J Trop Med Hyg 37 :640.

    • Search Google Scholar
    • Export Citation
  • 22

    Gubler DJ, Sather GE, Kuno G, Cabral JR, 1986. Dengue 3 virus transmission in Africa. Am J Trop Med Hyg 35 :1280–1284.

  • 23

    Rosen L, Gubler DJ, 1974. The use of mosquitoes to detect and propagate dengue viruses. Am J Trop Med Hyg 23 :1153–1160.

  • 24

    Gómez FE, Suárez CMM, Cardenas RC, 2001. Spa: Factores que modificam los índices larvários de Aedes aegypti en Colima, Mexico. Rev Panam Salud Publica 10 :6–12.

    • Search Google Scholar
    • Export Citation

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

APPLICATION OF AN ALTERNATIVE AEDES SPECIES (DIPTERA: CULICIDAE) SURVEILLANCE METHOD IN BOTUCATU CITY, SÃO PAULO, BRAZIL

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  • 1 Laboratório de Entomologia Molecular, Departamento de Parasitologia, Instituto de Biociências, Universidade Estadual Paulista, Botucatu, São Paulo, Brazil; Equipe de Controle de Zoonoses, Secretaria Municipal de Saúde, Botucatu, São Paulo, Brazil

One of the main problems with dengue is the control of Aedes aegypti, its major vector. In Brazil, the current control program for Ae. aegypti and Aedes albopictus populations includes larval density surveys. An interesting alternative is the use of a distinct index, the Premise Condition Index (PCI). This tool relates conditions of property, such as houses and yards, and the degree of shade with the occurrence of Aedes sp. oviposition, and is calculated as scores from 3 to 9. The lowest score indicates property in good condition and an unfavorable breeding environment, while the highest score indicates property at high risk for infestation by Aedes sp. The present study is based on the application of the PCI in an urban area of Botucatu, Brazil to confirm its effectiveness.

Dengue is the most important vector-borne viral disease in tropical countries, with at least 100 million cases reported each year.1 In Brazil, infection by the dengue virus has increased significantly in the last two decades after the reintroduction of mosquito vector Aedes (Stegomyia) aegypti (L.). Sympatric presence of Ae. aegypti and Aedes (Stegomyia) albopictus (Skuse) generates a new problem for dengue epidemiology. Aedes albopictus was first observed in Brazil in 1986, in the states of Espírito Santo, Minas Gerais, Rio de Janeiro, and São Paulo.2 Currently, this species is found in several states in this country. In some municipalities of Minas Gerais that reported Ae. aegypti in previous years, health workers have observed that Ae. albopictus is now the principal mosquito species.3 Aedes albopictus dissemination is due mainly to the international shipping trade of used tires, which provides an ideal mechanism for passive dispersion of immature stages.4,5

The presence of Ae. albopictus is a serious public health problem. First, it plays an important role in the transmission of several arboviruses and its susceptibility to these viruses is even greater than that of Ae. aegypti.6 Second, the species maintains the possibility of vertically transmitting serotypes 2 and 3 of the dengue virus naturally.7 Additionally, the mosquito shows aggressive anthropophilic behavior and a great adaptability to different habitats.8,9 This success is perhaps due to extreme variation in its adaptative traits, such as diapause10 and hardiness to cold temperatures.11

Epidemiologic surveillance associated with vector control remains the only way to prevent dengue outbreaks since an effective vaccine is not available.12,13 Surveillance is conducted by the determination of different indices that take into account the number of immature and mature forms of the mosquito. In Brazil, the current control program applied by the National Health Foundation/Ministry for Health for Ae. albopictus and Ae. aegypti populations is a set of concomitant and integrated epidemiologic surveillance, vector elimination, and social, environmental, and medical assistance. There are many problems that compromise the reliability of entomologic surveys. To obtain these indices, it is necessary to enter houses. In localities with ≥ 5,000 houses, 10% need to be surveyed (National Health Foundation, 2001).14 These methodologies require time, money, and trained personnel. However, it is occasionally difficult to enter houses, which decreases the significance of the index.

An interesting alternative is the use of a distinct index known as the Premise Condition Index (PCI).15 This tool relates the condition of property, such as the house and the yard, and the degree of shade, to the occurrence of Aedes sp. oviposition. The calculation of the PCI is achieved by the association of the three property variables (house, yard, and shade) calculated in scores from 3 to 9. The lowest score indicates property in good condition and an unfavorable breeding environment, while the highest score indicates property at high risk for infestation with to Aedes sp. The present study tested this instrument in an urban area of Botucatu, Brazil to confirm its effectiveness.

With the assistance of the Municipal Secretary for Health of Botucatu, we divided the city into 105 quadrants that covered its entire area. Houses (one per quadrant) were randomly chosen at the time of the visit. House conditions were recorded according Tun-Lin and others.15 After choosing and qualifying the house, one ovitrap was set up, with the home owner’s consent, in a peridomociliar environment, preferably in the garden in a shady place. When this was not possible, the ovitrap was placed in the patio. An ovitrap consisted of a black plastic container filled with water, with a wooden stick to collect eggs. Eggs from positive traps were induced to eclosion in the laboratory. Differentiation between species was carried out on adult forms by thoracic markings according to morphologic keys of Forattini.16 For the purpose of finding a significant association for the three property variables (house, yard, and shade), PCI scores (3–9) were compared with the presence or absence of Aedes eggs.

The occurrence of Ae. albopictus eggs showed a uniform distribution all over the city (41 of 105 ovitraps). Two ovitraps had only Ae. aegypti eggs, and 11 ovitraps had eggs from both species. When houses were grouped according to similar PCIs (Table 1), 65% of those with scores of 8 and 9 (considered to be houses in the worst condition) were positive with the presence of eggs, while only 19% of the properties with scores of 3 and 4 (houses in excellent condition) were positive. There was a positive correlation (r = 0.9684, P < 0.01) between house condition and percentage of positive houses, which clearly showed the usefulness of this method.

This preliminary analysis has demonstrated the accuracy of the PCI method, since most of the Aedes sp. were observed in properties with the highest PCT scores. Larval surveys conducted inside the same houses at the time of the PCT survey showed that 72% of the larva-positive houses were also positive for eggs. Only 4% of the houses had positive results in the larval survey, but were negative for the presence of eggs.

Ovitraps have been successfully used for detection of Aedes sp. in many countries.17 In Brazil, superior performance has been shown in comparison to larval surveys.18 Braga and others17 showed that that in 2,944 houses inspected, 7.5% were positive by larval survey while 25.1% were positive by ovitraps. Thus, to determine the degree of infestation of this vector in the city, the trap method was used in our study. Unexpectedly, the predominant mosquito was Ae. albopictus, not Ae. aegypti.

Aedes albopictus was found all over the city, including the downtown (urban) area. This is an important finding for municipal epidemiology because Ae. albopictus has been shown to maintain a dengue epidemic.19 Although it is not considered important in virus transmission to humans, this species is able to sustain the virus in nature due to high rates of trans-ovarian transmission.20 This reinforces other hypotheses2123 that the virus in semi-rural, rural, and forest areas could be sustained by a vector more efficient than Ae. aegypti by combining transovarian transmission and periodic presence in human and primate populations.

The present study showed the effectiveness of the PCI because worse conditions in houses showed a higher correlation with the presence of Aedes mosquitoes than in well-maintained houses. However, further studies should be undertaken to improve the technique, essentially to obtain a clearer distinction between intermediate and high PCI scores. Gómez and others24 also tested the PCI and showed its accuracy with other factors related to mosquito breeding. This does not mean that if sufficient resources are available, houses with lower PCI scores should be neglected. However, it does provide guidelines for locating houses that have been shown to contain most of the eggs. The major advantage of the PCI is that it offers a rapid assessment method for selecting houses for survey. Conversely, the PCI method requires specific training of health workers, since estimation of index parameters is reasonably subjective. In the case of dengue outbreaks, by having all representative house indices of the region, it will be much easier and less expensive to control the epidemic.

Table 1

Correlation between house condition and positive houses for Aedes albopictus eggs

House condition*Number of houses surveyedPositive houses (egg presence)Positive houses (%)
* Houses were grouped conforming their premise condition index (PCI): excellent (PCI = 3 and 4); good (PCI = 5); regular (PCI = 6); bad (PCI = 7); worst (PCI = 8 and 9).
Excellent21419
Good13538
Regular191052
Bad181161
Worst342265

*

Address correspondence to Paulo E. M. Ribolla, Departmento de Parasitologia, Instituto de Biociências, Universidade Estadual Paulista, Botucatu, São Paulo, Brazil. E-mail: pribolla@ibb.unesp.br

Authors’ addresses: Letícia A. Nogueira, Letícia T. Gushi, Newton G. Madeira, and Paulo E. M. Ribolla, Laboratório de Entomologia Molecular, Departamento de Parasitologia, Instituto de Biociências, Universidade Estadual Paulista, PO Box 510, 18618-000, Botucatu, São Paulo, Brazil. João E. Miranda, Equipe do Controle de Zoonoses, Secretaria Municipal da Saúde, Rua Major Matheus, 07 Vila dos Lavradores, 18609-083, Botucatu, São Paulo, Brazil.

Acknowledgments: We thank the Municipal Secretary for Health for their help in collecting field material. Paulo Eduardo Martins Ribolla is a fellow of the Conselho Nacional de Desenvolvimento Científico e Tecnológico.

Financial support: This study was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (Proc. No. 01/06647-9).

REFERENCES

  • 1

    McBride WJ, Bielefelted-Ohmann H, 2000. Dengue viral infections; pathogenesis and epidemiology. Microbes Infect 2 :1041–1050.

  • 2

    Forattini OP, 1986. Identificação de Aedes (Stegomyia) albopictus (Skuse) no Brasil. Rev Saude Publica 20 :244–245.

  • 3

    Ayres CF, Romao TP, Melo-Santos MA, Furtado AF, 2002. Genetic diversity in Brazilian populations of Aedes albopictus.Mem Inst Oswaldo Cruz 97 :871–875.

    • Search Google Scholar
    • Export Citation
  • 4

    Reiter P, Sprenger D, 1987. The used tire trade: a mechanism for the worldwide dispersal of container breeding mosquitoes. J Am Mosq Control Assoc 3 :494–501.

    • Search Google Scholar
    • Export Citation
  • 5

    Craven RB, Eliason DA, Francy DB, Reiter P, Campos EG, Jakob WL, Smith GC, Bozzi CJ, Moore CG, Maupin GO, Monath TP, 1988. Importation of Aedes albopictus and other exotic mosquito species into the United States in used tires from Asia. J Am Mosq Control Assoc 4 :138–142.

    • Search Google Scholar
    • Export Citation
  • 6

    Mitchell CJ, 1995. The role of Aedes albopictus as an arbovirus vector. Parassitologia 37 :109–113.

  • 7

    Ibanez-Bernal S, Briseno B, Mutebi JP, Argot E, Rodriguez G, Martinez-Campos C, Paz R, de la Fuente-San Roman P, Tapia-Conyer R, Flisser A, 1997. First record in America of Aedes albopictus naturally infected with dengue virus during the 1995 outbreak at Reynosa, Mexico. Med Vet Entomol 11 :305–309.

    • Search Google Scholar
    • Export Citation
  • 8

    Miller BR, Ballinger ME, 1988. Aedes albopictus mosquitoes introduced into Brazil: vector competence for yellow fever and dengue viruses. Trans R Soc Trop Med Hyg 82 :476–477.

    • Search Google Scholar
    • Export Citation
  • 9

    Rodhain F, 1995. Aedes albopictus: a potential problem in France. Parassitologia 37 :115–119.

  • 10

    Hawley WA, Pumpuni CB, Brady RH, Graig GB Jr, 1989. Overwintering survival of Aedes albopictus (Diptera: Culicidae) eggs in Indiana. J Med Entomol 26 :122–129.

    • Search Google Scholar
    • Export Citation
  • 11

    Hanson SM, Graig GB Jr, 1994. Cold acclimation, diapause, and geographic origin affect cold hardiness in eggs of Aedes albopictus (Diptera: Culicidae).J Med Entomol 31 :192–201.

    • Search Google Scholar
    • Export Citation
  • 12

    Rawlins SC, Martinez R, Wiltshire S, Legall G, 1998. A comparision of surveillance systems for the dengue vector Aedes aegypti in Port of Spain, Trinidad. J Am Mosq Control Assoc 14 :131–136.

    • Search Google Scholar
    • Export Citation
  • 13

    Pontes RJ, Freeman J, Oliveira-Lima JW, Hodgson JC, Spielman A, 2000. Vector densities that potentiate dengue outbreaks in a Brazilian city. Am J Trop Med Hyg 62 :378–383.

    • Search Google Scholar
    • Export Citation
  • 14

    Ministério da Saúde: Fundação Nacional da Saúde, 2001. Dengue Instruções para Pessoal de Combate ao Vetor: Manual de Normas Técnicas. Revised third edition. Brasília: Ministério da Saúde: Fundação Nacional da Saúde.

  • 15

    Tun-Lin W, Kay BH, Barnes A, 1995. The premise condition index: a tool for streamlining surveys of Aedes aegypti.Am J Trop Med Hyg 53 :591–594.

    • Search Google Scholar
    • Export Citation
  • 16

    Forattini OP, 2002. Culicidologia Médica. Volume 2. São Paulo: Editora da Universidade de São Paulo, 411–415.

  • 17

    Braga IA, Gomes AC, Nelson M, Mello RCG, Bergamaschi DP, Souza JMP, 2000. Comparação entre pesquisa larvária e armadilha de oviposição, para detecção de Aedes aegypti.Ver Soc Bras Med Trop 33 :347–353.

    • Search Google Scholar
    • Export Citation
  • 18

    Marques CCA, Marques GRAM, Brito M, Santos-Neto LG, Ishibashi VC, Gomes FA, 1993. Estudo comparativo de eficácia de larvitrampas e ovitrampas para vigilância de vetores de dengue e febre amarela. Rev Saude Publica 27 :237–241.

    • Search Google Scholar
    • Export Citation
  • 19

    Serufo JC, Oca HM, Tavares VA, Souza AM, Rosa RV, Jamal MC, Lemos JR, Oliveira MA, Nogueira RMR, Schatzmayr HG, 1993. Isolation of dengue virus type 1 from larvae of Aedes albopictus in Campos Altos City, state of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 88 :503–504.

    • Search Google Scholar
    • Export Citation
  • 20

    Shroyer DA, 1990. Vertical maintenance of dengue-1 virus in sequential generation of Aedes albopictus.J Am Mosq Control Assoc 6 :312.

  • 21

    Freier JE, Rosen L, 1987. Vertical transmission of dengue viruses by mosquitoes of the Aedes scutellaris group. Am J Trop Med Hyg 37 :640.

    • Search Google Scholar
    • Export Citation
  • 22

    Gubler DJ, Sather GE, Kuno G, Cabral JR, 1986. Dengue 3 virus transmission in Africa. Am J Trop Med Hyg 35 :1280–1284.

  • 23

    Rosen L, Gubler DJ, 1974. The use of mosquitoes to detect and propagate dengue viruses. Am J Trop Med Hyg 23 :1153–1160.

  • 24

    Gómez FE, Suárez CMM, Cardenas RC, 2001. Spa: Factores que modificam los índices larvários de Aedes aegypti en Colima, Mexico. Rev Panam Salud Publica 10 :6–12.

    • Search Google Scholar
    • Export Citation

Author Notes

Reprint requests: Paulo E. M. Ribolla, Departamento de Parasitologia, Instituto de Biociências, Universidade Estadual Paulista, Botucatu, São Paulo, Brazil, Telephone: 55-14-3811-6239, Fax: 55-14-3811-6239, E-mail: pribolla@ibb.unesp.br.
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